Ibironke, Josephine O.*; Friedman, David S.†; Repka, Michael X.‡; Katz, Joanne§; Giordano, Lydia*; Hawse, Patricia∥; Tielsch, James M.¶
Vision is important in development because it allows children to interact with their environment. Vision in preschool children is uniquely important because their visual system is still developing and they are at risk of developing amblyopia from some forms of uncorrected high ametropia or anisometropia.1 Deprivation may lead to long-term visual impairment.2,3
The presence of uncorrected refractive errors and an associated deficit in vision may be difficult to identify in young children. A vision deficit could be perceived by parents to be a problem with general development. Parents frequently discuss concerns about their child's development with the pediatrician.4–6 Such concerns, if carefully elicited, have been found predictive of developmental problems in children; with 80% sensitivity and 94% specificity.7 However, there is limited information evaluating the association between parental concerns about development and refractive errors in preschool children.
The Baltimore Pediatric Eye Disease Study (BPEDS) was a cross-sectional, population-based study to determine the prevalence of and risk factors for ocular disorders in urban preschool children. The purpose of this report is to examine whether parental concerns about development as assessed by the Parents' Evaluation of Developmental Status (PEDS) instrument were associated with significant refractive errors in preschool children.
BPEDS was designed to estimate and compare the prevalence of decreased vision, strabismus, amblyopia, and refractive error in a population-based sample of white and African American children aged 6 through 71 months living in Baltimore. Detailed methods and results have been published previously.8–10 All study activities were approved by the Committee on Human Research at the Johns Hopkins Bloomberg School of Public Health, the Battelle Centers for Public Health Research and Evaluation Institutional Review Board, and the Institutional Review Board of the Maryland Department of Health and Mental Hygiene.
The study enrolled subjects from 54 contiguous census tracts in northeastern and eastern Baltimore City and adjacent portions of Baltimore County, Maryland. In households with eligible children, an adult resident answered a questionnaire about basic demographic information, socioeconomics of the household, and the eye health of each eligible child. Eligibility criteria were (1) age 5 to 70 months on the day of the household screening and (2) parent or legal guardian confirmation that the subject resided in one of the selected BPEDS census tracts.
Enrolled subjects were invited for comprehensive eye examinations at a centrally located clinic. The examinations were performed by study-certified ophthalmic technicians and pediatric-trained optometrists or ophthalmologist.8–10 At the clinic, the parent or guardian (hereafter called parent) participated in a detailed interview about their child/children that covered (1) health care coverage and use, (2) basic medical history, (3) ocular history, (4) pregnancy and neonatal history, (5) tobacco and alcohol use during pregnancy, (6) presence or absence of developmental delay, (7) motor milestones, (8) socioeconomic status, and (9) the PEDS.11
Determination of Refractive Error
Cycloplegic autorefraction was attempted on all children using the handheld Retinomax autorefractor (RIGHT Medical, Virginia Beach, VA). Cycloplegia was attained by administering 1 drop of 0.5% proparacaine, 1 drop of cyclopentolate (0.5% if the child was 1 year or younger and 1.0% if the child was older than 1 year), and 1 drop of 2.5% phenylephrine. One additional drop of cyclopentolate was administered after waiting 5 min. The presence of cycloplegia was confirmed 30 min after the second drop with dynamic streak retinoscopy. A third drop of cyclopentolate was administered to those children with persistent accommodation as observed by the fluctuation of the retinoscopic reflex.
A Retinomax confidence level of 8 or greater was required for the measurement to be accepted.12 A maximum of three attempts were performed. If the confidence level could not be attained, a study-certified optometrist or ophthalmologist performed cycloplegic streak retinoscopy in a dim room with the child fixating on a distant target. For children with manifest strabismus, the fellow eye was occluded while performing the retinoscopy to prevent off-axis measurements. Children who were not cyclopleged were excluded from this analysis.
Based on a preanalysis consensus of the investigators, cut-points for significant refractive error were defined as hyperopia ≥3.00 diopters (D), myopia ≥1.00 D or astigmatism ≥1.50 D in either eye, or anisometropia ≥2.00 D. In addition, other cut-points of hyperopia ≥1.00 D, hyperopia ≥4.00 D, myopia ≥3.00 D, astigmatism ≥3.00 D, and anisometropia ≥1.00 D were also evaluated. The right eye and left eye spherical equivalent, right eye and left eye spherical powers, and the right eye and left eye cylinder powers were also treated as continuous variables during analysis.
Developmental Status Assessment
PEDS is a sensitive and well-validated instrument for developmental screening, with good psychometric properties.4,6 It has been proven useful regardless of socioeconomic status, educational level, and other parental factors.4 It has a sensitivity of 74 to 79% for the detection of developmental problems in children from birth to 8 years, with a specificity of 70 to 80%.4,5
The PEDS 10-item questionnaire was administered during the BPEDS clinic interview. Parents responded to questions about their child's learning, development, and behavior by answering “yes,” “no,” or “a little” to the questions (Table 1). Parents were asked to elaborate if they answered “yes” or “a little.” Parental concerns were compiled and the subjects assigned to five levels (A, B, C, D, or E) of risk for developmental problems according to the PEDS scoring protocol.11 For the purpose of this project, the five categories of a child's risk were collapsed into high- and low-risk groups. Children assigned to levels A or B were classified as having high risk for developmental problems. All other children were classified as having low risk for developmental problems (Table 2).
All statistical analyses were performed using the STATA 10 (StataCorp, College Station, TX).13 Demographic and health characteristics of the children in the high- and low-risk groups were compared using the two sample t-test for continuous variables, whereas non-continuous variables were compared using the χ2. Factors that were significantly different between the high- and low-risk groups were included in the multiple logistic regression analysis to determine their influence on any relationship between parental concerns about development and the presence of refractive errors. Crude odds ratios [OR] and 95% confidence intervals [CI] of the association between parental concerns and the preset cut-points for each refractive error were calculated. Multiple logistic regression was used to estimate the OR after adjusting for age, sex, ethnicity, history of an eye problem, current eye health, primary caregiver's education, age of mother, age of father, smoking during pregnancy, and the relationship of the primary caregiver. A multiple logistic regression was also used to calculate the OR of parental concerns when refractive error was treated as a continuous variable. The t-test was used to determine if refractive error means were different in the high- and low-risk groups. All reported p-values were two tailed. Analyses were repeated comparing children older than 36 months to children 36 months and younger.
BPEDS identified 4132 preschool-aged children, 3990 eligible children (97%) were enrolled, and 2546 children (62%) were examined.8 The PEDS interviews were completed by 2499 children (60%). Of these children, 118 children were excluded because their refractive errors were measured without cycloplegia. The remaining 2381 children represent the cohort for this report.
There were 1158 males (48.6%) and 1223 females (51.4%). The mean age of the children included was 38.5 months [standard deviation (SD), 18.4], the median age was 39 months, the minimum age was 6 months, and the maximum age was 71 months. Nine hundred fifty-one (40.0%) were white, 1197 (50.3%) were African American, and 203 (9.7%) were from other ethnic groups (Table 3). An eye problem had been previously diagnosed in 102 children, whereas parents of three children were uncertain. For 61 children, the problem was a need for glasses. Only 43 children already had glasses, whereas 18 were without glasses.
On average, mothers were 30.6 years of age and fathers were 35.8 years of age at the time of the interview. Mothers were the respondents for 80.4%, biological fathers for 7.8%, and guardians for 11.8%.The average and the median years of education of the primary caregiver were 13.3 and 10.5 years, respectively. The proportion of families with incomes greater than $20,000 was 63.9%.
Demographic characteristics, including the child's age, sex, maternal and paternal age, history of eye problems, current eye health, existing developmental delay concerns (as reported by the caregiver), type of health insurance, household income, smoking during pregnancy and the primary caregiver's education were significantly associated with parental concerns determined from the PEDS (Table 3). However, only age, sex, maternal age, and smoking during pregnancy were associated with refractive errors.
The PEDS found 510 children [21.4%, standard error (SE), ±0.008, 95% CI: 19.8 to 23.1] at high risk for developmental problems based on parental concerns. The mean age of the high-risk group was 43.4 months (SD, 16.2), the median age was 45 months, the minimum age was 7 months, and the maximum age was 71 months. Of the 510 children in the high-risk group, 199 were males (39.0%). At low risk were1871 children (78.6%; SE ±0.008; 95% CI: 76.9 to 80.2). The mean age of the children in the low-risk group was 37.1 months (SD, 18.7), the median age was 37 months, the minimum age was 6 months, and the maximum age was 71 months.
There were 1277 children older than 36 months with a mean age of 53.3 months (SD, 9.4). Among these older children, 329 were in the high-risk group with the mean age of 53.5 months (SD, 9.4). Males accounted for 124 (37.7%). The mean age of the 948 children in the low-risk group was 53.2 months (SD, 9.4). There were 1104 children aged 36 months or younger; the mean age was 21.4 months (SD, 8.9). Among the younger children, 180 were in the high-risk group; the mean age in the high-risk group was 25.0 months (SD, 7.3). Males accounted for 41.7%. Nine hundred twenty-two of the children 36 months or younger were in the low-risk group; the mean age was 20.6 months (SD, 9.1) (Table 3).
Based on the study's preselected cut-points for significant refractive errors, 232 children had hyperopia ≥3.00 D; 23.7% were in the high-risk group for developmental problems compared with 21.3%. For the 112 children with myopia ≥1.00 D, 25.0% were in the high-risk group compared with 21.4%. For the 292 children with astigmatism ≥1.50 D, 26.7% were in the high-risk group compared with 21.0%. Twenty-two children had anisometropia ≥2.00 D, 40.9% were in the high-risk group compared with 21.4% in those anisometropia <2.00 D. There was no evidence of an effect modification by sex in the associations of developmental concerns with refractive error, because the higher prevalence of developmental concerns in females was consistent for all refractive errors (Table 4).
After adjusting for age, sex, current health, previous diagnosis of an eye problem, primary caregiver's education, age of mother, age of father, smoking during pregnancy, and the relationship of the primary caregiver, parents of children with hyperopia ≥3.00 D or myopia ≥1.00 D in either eye were not statistically more likely to have concerns about their child's development (Table 5). However, parents of children with significant astigmatism ≥1.50 D were statistically more likely to have concerns about their child's development (OR = 1.44; 95% CI: 1.08 to 1.93). The association of parental concerns with significant astigmatism was irrespective of the type of astigmatism (with-the-rule, against-the-rule, or oblique). Parents of children with anisometropia ≥2.00 D were also more likely to have developmental concerns (OR = 2.61; 95% CI: 1.07 to 6.34).
We identified no association between parental concerns when additional cut-points were considered (hyperopia ≥1.00 D, hyperopia ≥4.00 D, myopia ≥3.00 D, astigmatism ≥3.00 D, and anisometropia ≥1.00 D) (Table 5). The association between parental concerns and significant refractive error was stronger in children older than 36 months (Table 6). This was most evident for hyperopia, astigmatism, and anisometropia.
In addition, when children assigned to PEDS levels A, B, and C were classified as the high-risk group, only parents of children with astigmatism ≥1.50 D had statistically significant concerns. The right eye spherical equivalent minimum, maximum, median, and mean were −8.75, +10.875, 1.00, and 1.08, respectively. There was no association with increase in spherical equivalent and spherical power in either eye, but the spherical equivalent in both eyes was associated in children older than 36 months.
We found parental concerns about their child's development to be associated with some refractive errors in this urban population of preschool children. Parents of preschool children with astigmatism (≥1.50 D) or anisometropia (≥2.00 D) were more likely than other parents to have concerns about developmental problems. Myopia was not associated with parental concerns. Parents of children aged 36 through 71 months with hyperopia ≥3.00, astigmatism ≥1.50 D, or anisometropia ≥2.00 D were more likely to have concerns about development.
Parental concerns in our cohort were more prevalent in children older than 36 months compared with younger children. However, the PEDS instrument generally finds that parents of older children have more concerns.4 The odds of parental concerns may also be increased in older preschool children because problems may be more noticeable because their visual demands are more than likely different from younger children.
In addition, more parents of girls than boys had concerns that put them in the high-risk group for developmental problem, and more girls had significant refractive errors (Tables 3 and 4). This gender bias is not consistent with PEDS validation data that show that boys are more often in the high-risk groups.4,5 Our observation lends additional support to the association of developmental concerns and refractive error.
There was no difference in parental concerns by ethnicity. This is consistent with validation data of the PEDS instrument.4 Maternal and paternal ages were higher in the high-risk group. These findings are also consistent with PEDS validation data.
Significant uncorrected refractive errors are risk factors for amblyopia.2 Uncorrected refractive errors have also been associated with abnormal development,14–17 including reduced cognitive ability,14,15 and motor skill,15,16 in infants and preschool-aged children. Deficits in these skills and difficulties could be perceived as developmental problems by parents.
When all the preschool children in this study were considered, there was no association found between parental concerns about developmental problems and hyperopia. However, when children older than 36 months were compared with younger children, parental concerns were significantly more likely in these older children if they had hyperopia ≥3.00 D. Some studies have shown that hyperopia is associated with visuomotor and visuocognitive development in children.14–17 Roch-Levecq et al.14 found that preschool children aged 3 to 5 years with uncorrected bilateral hyperopia ≥4.00 D had significantly reduced visual-motor integration when compared with emmetropic children. Atkinson et al. performed a longitudinal study comparing infants with significant hyperopia (≥3.50 D in one meridian) with infants with normal refractive errors. They found that hyperopic children showed mild, but consistent delays in visuocognitive and visuomotor development that continued to age 5 years15,16 and age 7 years.17 It is possible that the parental developmental concerns manifest when older hyperopic preschool children do not acquire or master visually based skills.
There was no association found between myopia (≥1.00 D or ≥3.00 D) and parental concerns about developmental problems in this population of preschool children. Perhaps, the near working distance for children protects them.1 Alternatively, parents may not perceive any developmental concerns because problems associated with uncorrected myopia common in school settings are not apparent in preschool children.
Astigmatism ≥1.50 D was significantly associated with parental concerns about development in preschool children. This association was stronger in children older than 36 months when they were compared with younger children. Preschool children age 3 to 5 with uncorrected astigmatism ≥1.50 D have been shown to have deficits in grating acuity and could lead to amblyopia.18,19 Children with astigmatism ≥2.00 D in 3 year olds or ≥1.50 D in 4 year olds have also been shown to have visual motor integration deficits.14 These deficits could be perceived as developmental problems.
Anisometropia ≥2.00 D was associated with parental concerns about developmental problems in this population of preschool children, especially among children aged 36 through 71 months. Parental concerns may arise in children with anisometropia ≥2.00 D because children with higher amounts may develop amblyopia which may lead to vision problems that parents perceive as developmental problems. There was no association between parental concerns and lesser anisometropia ≥1.00 D, possibly because the visual impairment in one eye is too mild to produce a developmental deficit.1,20,21
Increased amounts of anisometropia have been found to be associated with reduced binocularity in children.22 Poor binocularity could be perceived as a developmental problem by the parents. It is also possible that anisometropia is a marker for some other factors that may put a child at higher risk for developmental delay, but we could not assess this in BPEDS.
When there is a parental concern about development, further screening, diagnostic tests, and referrals are recommended to identify children with true developmental delays that need early intervention.4,23 Pediatricians may consult neurologists, occupational therapists, physical therapists, social workers, psychologists, and speech therapists.4,6 This report suggests that if there are parental concerns about development in a preschool child, an eye examination with cycloplegic refraction should be considered to detect significant refractive errors.
There are several strengths of this study. A comprehensive eye examination was performed and refractive errors were accurately determined with automated refraction under cycloplegia by study-trained testers. The PEDS tool has been previously validated and the full tool was included so parental concerns about development could be adequately examined. Examiners were masked to the PEDS results and parents were masked to their child's refractive error.
There are important limitations of the study. This study cannot prove a causal relationship between refractive error and parental concerns about developmental delay. The PEDS questions were included late in the interview and parent responses could have been influenced by earlier demographic and health questions. Because of the cross-sectional design, parental concerns were not re-evaluated after correction of refractive error, to determine if these changed. Only one developmental screening tool was used; no other tools or examinations were used to confirm the presence or absence of developmental problems. The response rate to examination was relatively low, at 64% of those eligible. It is not known how those who did not present for the eye examination might have been categorized by the PEDS nor is it known whether the association between developmental risk and ocular outcomes would have been stronger or weaker in this group.
This study found that parental concerns about development are associated with significant refractive error in this preschool population aged 6 to 71 months, especially among those children aged 36 through 71 months. Parental concerns may be more significant in older children because visual and developmental demands are greater. Because of the potential consequences of uncorrected refractive errors, children whose parents have expressed concerns regarding development should be examined with cycloplegic refraction for refractive errors.
We thank the members of the Data Monitoring and Oversight Committee, Drs. Eileen Birch, Karen Cruickshanks, Jonathan Holmes (chair), Natalie Kurinij (NEI ex-officio), Maureen Maguire, Joseph Miller, Graham Quinn, and Karla Zadnik, for their help in completing this study. We also thank Jiangxia Wang, MS, MA (Wilmer Biostatistics Consulting Center) for providing her biostatistics expertise.
David S. Friedman
Wilmer Eye Institute, Wilmer 120
600 North Wolfe Street
Baltimore, Maryland 21287
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